Repeated transspinal stimulation decreases soleus H-reflex excitability and restores spinal inhibition in human spinal cord injury

Abstract

Transcutaneous spinal cord or transspinal stimulation over the thoracolumbar enlargement, the spinal location of motoneurons innervating leg muscles, modulates neural circuits engaged in the control of movement. The extent to which daily sessions (e.g. repeated) of transspinal stimulation affects soleus H-reflex excitability in individuals with chronic spinal cord injury (SCI) remains largely unknown. In this study, we established the effects of repeated cathodal transspinal stimulation on soleus H-reflex excitability and spinal inhibition in individuals with and without chronic SCI. Ten SCI and 10 healthy control subjects received monophasic transspinal stimuli of 1-ms duration at 0.2 Hz at subthreshold and suprathreshold intensities of the right soleus transspinal evoked potential (TEP). SCI subjects received an average of 16 stimulation sessions, while healthy control subjects received an average of 10 stimulation sessions. Before and one or two days post intervention, we used the soleus H reflex to assess changes in motoneuron recruitment, homosynaptic depression following single tibial nerve stimuli delivered at 0.1, 0.125, 0.2, 0.33 and 1.0 Hz, and postactivation depression following paired tibial nerve stimuli at the interstimulus intervals of 60, 100, 300, and 500 ms. Soleus H-reflex excitability was decreased in both legs in motor incomplete and complete SCI but not in healthy control subjects. Soleus H-reflex homosynaptic and postactivation depression was present in motor incomplete and complete SCI but was of lesser strength to that observed in healthy control subjects. Repeated transspinal stimulation increased homosynaptic depression in all SCI subjects and remained unaltered in healthy controls. Postactivation depression remained unaltered in all subject groups. Lastly, transspinal stimulation decreased the severity of spasms and ankle clonus. The results indicate decreased reflex hyperexcitability and recovery of spinal inhibitory control in the injured human spinal cord with repeated transspinal stimulation. Transspinal stimulation is a noninvasive neuromodulation method for restoring spinally-mediated afferent reflex actions after SCI in humans.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Soleus H-reflex recruitment curves before and after repeated transspinal stimulation in individuals with and without SCI.

Soleus H reflexes recorded at increasing stimulation intensities until the H reflex reached maximal amplitudes as a percentage of the Mmax are plotted against the predicted 50% of maximal H-reflex stimulus intensity (S50-Hmax) observed at baseline. Soleus H reflexes before (green) and after (black) cathodal transspinal stimulation are indicated separately for the left and right legs, and from both legs for AIS C-D, AIS A-B, and healthy control subjects. *p < .05, significant differences of reflexes recorded before and after stimulation. Error bars not indicated for clarity purposes.

Fig 2. Soleus M-wave recruitment curves before and after repeated cathodal transspinal stimulation in individuals with and without SCI.

Soleus M-wave sizes as a percentage of the Mmax are plotted against the predicted multiples of 50% of maximal M-wave stimulus intensity (S50-Mmax) for left and right legs grouped for AIS C- D, AIS A-B, and healthy control subjects. Error bars not indicated for clarity purposes.

Fig 3. Soleus H-reflex waveforms at different stimulation frequencies in an individual with chronic SCI.

Non-rectified waveform averages of soleus H reflexes recorded at different stimulation frequencies from an individual with SCI (R12—AIS D) in whom the soleus H reflex at 30% of the maximal M wave coincided with absent M wave.

Fig 4. Soleus H-reflex homosynaptic depression before and after cathodal repeated transspinal stimulation in individuals with and without SCI.

Soleus H reflexes evoked at different stimulation frequencies before (green) and after (black) repeated cathodal transspinal stimulation are indicated separately for the left, right and both legs combined for AIS C-D, AIS A-B, and healthy control subjects. On the abscissa, the stimulation frequency is indicated. Ordinate indicates the soleus H reflexes normalized to the H reflex evoked at 0.1 Hz. *p < .05, significant differences of reflexes recorded before and after stimulation. Error bars denote the SE.

Fig 5. Soleus H-reflex waveforms following paired stimulation in an individual with chronic SCI.

Non-rectified waveform averages of soleus H reflexes recorded upon paired tibial nerve stimuli from one individual with SCI (R12—AIS D) in whom the soleus H reflex at 30% of the maximal M wave coincided with absent M wave.

Fig 6. Soleus H-reflex postactivation depression before and after repeated cathodal transspinal stimulation in individuals with and without SCI.

Soleus H reflexes evoked upon paired tibial nerve stimuli before (green) and after (black) repeated cathodal transspinal stimulation are indicated separately for the left and right legs, and from both legs for AIS C-D, AIS A-B, and healthy control subjects. On the abscissa, the interstimulus interval (ISI) of paired tibial nerve stimuli is indicated. Ordinate indicates the soleus H reflexes evoked by the 2nd stimulus (H2) normalized to the mean amplitude of the H reflex evoked by the 1st stimulus (H1). *p < .05, significant differences of reflexes recorded across different ISIs. Error bars denote the SE.